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Decoding the Time-Dependent Response of Bioluminescent Metal-Detecting Whole-Cell Bacterial Sensors Jérôme F.L

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Decoding the Time-Dependent Response of Bioluminescent Metal-Detecting Whole-Cell Bacterial Sensors Jérôme F.L Decoding the Time-Dependent Response of Bioluminescent Metal-Detecting Whole-Cell Bacterial Sensors Jérôme F.L. Duval, Christophe Pagnout To cite this version: Jérôme F.L. Duval, Christophe Pagnout. Decoding the Time-Dependent Response of Bioluminescent Metal-Detecting Whole-Cell Bacterial Sensors. ACS Sensors, American Chemical Society, 2020, 309, pp.article 127751. 10.1021/acssensors.9b00349. hal-02095865 HAL Id: hal-02095865 https://hal.univ-lorraine.fr/hal-02095865 Submitted on 30 Apr 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Decoding the Time-Dependent Response of Bioluminescent Metal-Detecting Whole-Cell Bacterial Sensors Jérôme F.L. Duval,1, Christophe Pagnout2 1 Université de Lorraine, CNRS, LIEC (Laboratoire Interdisciplinaire des Environnements Continentaux), UMR7360, Vandoeuvre-lès-Nancy F-54501, France. 2 Université de Lorraine, CNRS, LIEC, UMR7360, Campus Bridoux, Metz F-57070, France. Corresponding author: [email protected] Abstract. The signal produced by aqueous dispersions of bioluminescent, metal-responsive whole-cell bacterial sensors is indicative of the concentration of bioavailable metal ions in solution. The conventional calibration-based strategy followed for measuring this concentration is however inadequate to provide any quantitative prediction of the cells response over time as a function of e.g. their growth features, their defining metal accumulation properties, or the physicochemical medium composition. Such an evaluation is still critically needed for assessing on a mechanistic level the performance of biosensors in terms of metal bioavailability and toxicity monitoring. Herein we report a comprehensive formalism unraveling how the dependence of bioluminescence on time is governed by the dynamics of metal biouptake, by the activation kinetics of lux-based reporter gene, by the ensuing rate of luciferase production, the kinetics of light emission and quenching. It is shown that bioluminescence signal corresponds to the convolution product between two time-dependent functions, one detailing the dynamic interplay of the above micro- and nanoscale processes, and the other pertaining to the change in concentration of photoactive cell sensors over time. Numerical computations illustrate how the shape and magnitude of the bioluminescence peak(s) are intimately connected to the dependence of the photoactive cells concentration on time and to the magnitudes of Deborah numbers that compare the relevant timescales of the biointerfacial and intracellular events controlling light emission. Explicit analytical expressions are further derived for practical situations where bioluminescence is proportional to the concentration of metal ions in solution. The theory is further quantitatively supported by experiments performed on luminescent cadmium-responsive lux-based Escherichia coli biosensors. Keywords. Whole-cell bacterial sensors, Bioluminescence, Time-dependent response, Dynamics, Metal biouptake, Luciferase, Quenching. 1 In a context where anthropogenic activities lead to significant contamination of natural aquatic environments, efficient ecosystem management strategies requires suitable devices to detect trace pollutants such as metals in aqueous solutions.1 Conventional physicochemical methods adopted for that purpose (e.g. spectrometry, conductivity, complexometry) often suffer from the complexity of sample preparation protocols, from interference effects associated with the aqueous matrix containing the element to be measured, or the impossibility to assess the bioavailable metal fraction, which is however essential for a proper estimate of toxicity effects on biota.2-6 In order to develop reliable methods for a fine monitoring of metals bioavailability and toxicity, the scientific community has resorted to solutions derived from biotechnologies, such as whole-cell microbial biosensors.7-10 The latter correspond to genetically modified microorganisms that emit a measurable physical or (electro)chemical signal in the presence of the target metal analyte.7-13 Genetic constructions are all based on the same principle and are strongly inspired by bacterial mechanisms of metal homeostasis.7 Reporter genes, introduced e.g. in the form of plasmids, are fused to a promoter whose expression is regulated by a regulatory (or repressor) protein that has a strong affinity with the metal element to be detected (Figure 1). In the absence of this element, the expression of reporter genes is repressed by the repressor attached to the promoter. Inactivation of the repressor occurs when the latter forms a complex with the metal ion, thus allowing the expression of reporter genes and the production of so-called reporter proteins (e.g. GFP or luciferase) at the origin of the measured signal (e.g. fluorescence or luminescence).7,8 Many so-constructed whole-cell bacterial sensors are listed in the literature12-18 with detection limits from a few nM to ten µM. The response of bacterial metal sensors over time depends on the intracellular concentration of the target metal and, more generically, on the dynamics of the processes that determine the partition of metals at the interphase between the biosensor and the extracellular medium.18 Depending on the bacterial systems considered and on medium composition, these processes include the reactive transfer of metals from the solution to the biosurface (e.g. their speciation),3,18-20 their passive biosorption,18 their internalization and bioaccumulation,21,22 or their excretion via efflux pumps.22 The biosensor signal is further intimately determined by the production rate of reporter proteins, which necessarily depends on the efficiency with which the transcription of reporter genes is activated by the metal ion-repressor protein complex.18,23-25 The physiology of cell sensors is an additional factor controlling their ability to produce light, and any interfering toxic effects generated by the metal species shall necessarily impact their response. These elements illustrate the complexity of the signal emitted by metal-responsive whole- cell bacterial sensors, the time dependence and magnitude of which are inherently mediated by interrelated extracellular, biointerfacial and intracellular bio-physicochemical processes. The ensuing lack of predictability of biosensor signals probably explains why this technology has met a limited number of 2 commercial achievements for environmental monitoring26,27 and why testing in natural aquatic media still remains scarce.12,17 Further efforts are thus required to rationalize whole-cell bacterial sensors signals on mechanistic and quantitative levels. The models developed for that purpose mainly rely on systems of differential equations that translate the coupling between kinetics of the successive steps leading to e.g. fluorescence or luminescence emission.18,23,28-31 As correctly argued in Ref. [23] where focus is given to bioluminescence, these models generally differ in their degree of sophistication for representing the various molecular determinants that control bioluminescence reaction and catalysis thereof, and thus in their number of introduced parameters, some of them remaining difficult -if not impossible- to measure under realistic sensors exposition conditions. With some exceptions,18 most of these approaches have in common that they further discard the complexity of the physicochemical processes governing the bioavailability of the target analyte at the biosensors/solution interface. The impact of cell growth on biosensors response is further sometimes incorrectly formulated by introduction of a simple proportionality factor in theoretical expressions of bioluminescence,24 which contrasts with the non- linearity recently invoked in the noticeable work by Delle Side et al.23 In line with the nature of the bio- system they considered, these authors did not account for the possible exchange fluxes of the molecules triggering light production, between cells and external medium. This aspect is however critical for proper assessment of the luminescence emitted by metal-responsive whole-cell biosensors.18 In view of the above elements, we report herein a conceptual framework allowing a full integration of the dynamic coupling between (i) the processes that regulate the partitioning of metals at the interphase between aqueous medium and luminescent metal-responsive whole-cell bacterial sensors, (ii) the formation of metal-repressor protein complex, which initiates reporter gene expression, (iii) the production of luciferase and the ensuing light emission and quenching, and finally (iv) the processes leading to time variations in concentration of photoactive cells. Illustrative numerical computations, supported by tractable analytical developments, decipher the impact of each of the above process on the bioluminescence response. Implications for bioluminescence data interpretation are further discussed, and analysis of the bioluminescence response of cadmium-detecting lux-based Escherichia coli biosensors supports theory.
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